Ecological and genomic insights into stick insect speciation

Studies of populations at different phases of speciation are beginning to illuminate the processes and genetic changes underlying the formation of new species. Our work on Timema stick insects suggests that speciation can be initiated by a few genetic changes that are associated with natural selection on colour-pattern loci. However, the overall process is multi-faceted and involves mate choice and genome-wide differentiation. Thus, substantial progress towards speciation may involve the alignment of multiple aspects of differentiation. (Riesch et al. 2017. Nat. Ecol. Evol. 1: 0086, DOI: 10.1038/s41559-017-0082)

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Speciation involves genetic differentiation. In the absence of gene
flow, genome-wide differentiation readily builds by selection and drift.
Differentiation with gene flow, however, is more complex. The genic
model (Wu 2001) predicts that speciation begins when a few genetic
regions subject to strong divergent natural or sexual selection become
resistant to gene flow, leading to peaks of localized genetic
differentiation in the genome. As speciation progresses, additional
genetic regions differentiate and the effects of reproductive isolation
become more genome-wide. Although this spectrum from localized to
genome-wide differentiation provides a conceptual and theoretical
framework for analysing speciation, empirical understanding of it is
limited (Seehausen et al. 2014). In particular, localized peaks of differentiation can arise due to numerous processes, some of which have little or nothing to do with reduced gene flow (Cruickshank and Hahn 2014), and thus the significance of such peaks for speciation per se remains unclear.

In this issue of Nature Ecology
and Evolution we report on transitions between phases of genomic
differentiation during speciation using data from >100 populations of
11 species of Timema stick insects (Riesch et al. 2017). The idea
behind this study dates back decades, when Cristina Sandoval and Bernie
Crespi recognized this group could harbour variation in phases of speciation.
I entered the system in the year 2000 and used experiments to estimate
reproductive isolation (Nosil et al. 2002). This largely involved driving around California
in my van, collecting Timema in their characteristic habitats (Figure
1), and conducting simple experiments on survival on different host
plants and mate preference. Over the years, as funding emerged, the
project became larger and more sophisticated (supported by the European
Research Council, the Human Frontiers Science Program, and the Natural
Sciences and Engineering Council of Canada). Collaborators joined in
(like Gerhard and Regine Gries) and the genomic and chemical ecology
elements were developed, led here by Zach Gompert and Rüdiger Riesch,
respectively. Today, we published results based on data collected
between 1996 and 2013, including >1000 re-sequenced whole genomes.

Figure
1: Chaparral near Santa Barbara, California. Timema
are
often found in this biome of dense
thickets and thorny bushes. Photo credit: R. Riesch.

Timema
differ
in their colours and colour-patterns, adaptations that confer
camouflage on their host plants against visual predators such as
birds (Sandoval 1994a, b, Nosil and Crespi 2006). We find
that, consistent with early phases of genic speciation,
colour-pattern loci reside in localized genetic regions of
accentuated differentiation between populations experiencing gene
flow. However, colour-pattern is controlled by few loci and does not affect mate choice, and thus divergence in this trait alone does not drive substantial progress towards speciation or genome-wide differentiation.

Instead, transitions to genome-wide differentiation with gene flow are associated with differentiation in polygenic
chemical traits affecting mate choice. Thus, intermediate phases of
speciation are associated with genome-wide differentiation and sexual mating isolation, but not growth of a few peaks or ‘islands’ in the genome.
Moreover, we find that complete sexual isolation takes very long to evolve such that other (yet to be thoroughly studied) reproductive barriers likely contribute to advanced stages of Timema speciation. Overall, the results suggest that substantial progress towards
speciation may involve the alignment of multi-faceted aspects of
differentiation.
We suspect similar conclusions may apply to other systems where
strong reproductive isolation involves many traits and evolves in a
polygenic fashion.

Although
many questions remain unanswered, it seems fairly certain that speciation in
this group involves more than divergence in cryptic coloration, and
our results point to mating isolation and other reproductive
barriers, as well as geographic separation, as being important. Thus,
the striking example of crypsis in Timema
shown
here (Figure 2) represents only one aspect of the multi-faceted
speciation process.

Nosil, P. and B. J. Crespi. 2006.
Experimental evidence that predation promotes divergence in adaptive
radiation. Proceedings of the National Academy of Sciences of the United
States of America 103:9090-9095.

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